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JACC: CARDIOVASCULAR IMAGING VOL. 11, NO.

11, 2018

ª 2018 BY THE AMERICAN COLLEGE OF CARDIOLOGY FOUNDATION

PUBLISHED BY ELSEVIER

Lung Ultrasound for the Cardiologist


Eugenio Picano, MD, PHD,a Maria Chiara Scali, MD, PHD,b Quirino Ciampi, MD, PHD,c Daniel Lichtenstein, MDd

ABSTRACT

For a cardiologist, lung ultrasound is an add-on to transthoracic echocardiography, just as lung auscultation is part of a
cardiac physical examination. A cardiac 3.5- to 5.0-MHz transducer is generally suitable because the small footprint
makes it ideal for scanning intercostal spaces. The image quality is often adequate, and the lung acoustic window is
always patent. The cumulative increase in imaging time is <1 min for the 2 main applications targeted on pleural water
(pleural effusion) and lung water (pulmonary congestion as multiple B-lines). In these settings, lung ultrasound out-
performs the diagnostic accuracy of the chest radiograph, with a low-cost, portable, real-time, radiation-free method. A
“wet lung” detected by lung ultrasound predicts impending acute heart failure decompensation and may trigger lung
decongestion therapy. The doctors of tomorrow may still listen with a stethoscope to their patient’s lung, but they will
certainly be seeing it with ultrasound. (J Am Coll Cardiol Img 2018;11:1692–705) © 2018 by the American College of
Cardiology Foundation.

LUNG ULTRASOUND IN CARDIOLOGY: neighboring or superimposed scanning fields on the


HISTORICAL BACKGROUND left anterior hemithorax. The diagnostic information
provided by lung ultrasound is of obvious clinical
Two hundred years after Laennec (1), who first interest to the cardiologist, who is well aware of the
introduced mediated lung auscultation as part of the prognostic and therapeutic relevance of extravascular
physical examination of the heart in 1819, the trans- lung water, and how a real-time assessment of lung
ducer follows the same pathway as the stethoscope, water may provide information complementary to
from the cardiac area to lung fields, with several conventional methods based on physical examination
diagnostic benefits in the same examination. This and chest radiographs to detect pulmonary conges-
may seem obvious now, but for our generation of tion. In addition, intensivists and cardiologists often
cardiologists it took 50 years of transthoracic echo- work on the same patients, and there is usually a
cardiography (TTE) practice before we shifted the close spatial proximity between the intensive care
transducer by a few centimeters from the cardiac and coronary units. This logistic setting should
acoustic window to gain a view of the amazing new theoretically facilitate the spread of innovative prac-
diagnostic world of lung ultrasound. tices. However, TTE and lung ultrasound remained
In the 1990s, lung ultrasound was first proposed divided for decades by an invisible but impenetrable
with pioneering applications in the critically ill in a cultural wall. Standard textbook knowledge told us
range of clinical conditions (2), including the detec- that the lung is filled with air (>90%), and air stops
tion of hemodynamic acute pulmonary edema (APE). the ultrasound signal because of the very high
It was only in 2004 that TTE was combined with lung impedance mismatch with chest tissues. The clinical
ultrasound to detect pulmonary congestion in pa- corollary was that “ultrasound imaging is not useful
tients with heart failure who were admitted to a car- for evaluation of pulmonary parenchyma” (4). In re-
diology ward (3). ality, the lung acoustic window is always open, even
In retrospect, the technological and cultural gap when the cardiac acoustic window for TTE is shut (5).
between TTE and lung ultrasound was very narrow Although only a limited portion of lung parenchyma
and did not require an intuitive mind to bridge it. The can be visualized, this minute portion is critically
2 techniques share the same equipment, with important because most acute life-threatening

From the aCNR Institute of Clinical Physiology, Pisa, Italy; bCardiology Department, Nottola Hospital, Siena, Italy; cCardiology
Division, Fatebenefratelli Hospital, Benevento, Italy; and the dMedical Intensive Care Unit, Ambroise-Paré Hospital, Paris-West
University, Boulogne, France. All authors have reported that they have no relationships relevant to the contents of this paper
to disclose.

Manuscript received January 25, 2018; revised manuscript received May 25, 2018, accepted June 19, 2018.

ISSN 1936-878X/$36.00 https://doi.org/10.1016/j.jcmg.2018.06.023


JACC: CARDIOVASCULAR IMAGING, VOL. 11, NO. 11, 2018 Picano et al. 1693
NOVEMBER 2018:1692–705 Heart-Driven Lung Ultrasound

disorders abut the pleural line: pleural effusions, be “kindergarten” in the echocardiography ABBREVIATIONS

pneumothorax, and acute interstitial syndrome in cursus studiorum, whereas the identification AND ACRONYMS

100% of cases; and lung consolidation in 98.5% of of regional wall motion abnormalities is the
AHF = acute heart failure
cases. more challenging “university” (7).
APE = acute pulmonary edema
Once the cultural wall of impedance bias sur- TRANSDUCER. The probe is applied perpen-
ARDS = acute respiratory
rounding ultrasound evaluation of the chest had dicular to the chest wall, in a sublongitudinal distress syndrome
fallen, cardiologists learned quickly what intensivists view following rib obliquity. The small foot- BLUE = bedside lung
had known for decades. Lung ultrasound (also called print of a cardiac transducer makes it espe- ultrasonography in emergency
thoracic ultrasound or chest sonography, but these cially suitable for scanning spaces between PLAPS = posterolateral
labels may include mediastinum and the heart) pro- ribs, and a 3.5- to 5.0-MHz frequency allows alveolar and/or pleural

vides a highly versatile and valuable diagnostic tool syndrome


adequate visualization of subpleural struc-
in many conditions that cardiologists encounter TTE = transthoracic
tures, although with limited resolution to
echocardiography
every day in their practice, from heart failure to pul- locate the pleural line with confidence. Crit-
monary embolism. The information on lung water can ical care physicians increasingly use 5-MHz micro-
be easily obtained at baseline and by serially convex probes that give a better view of the whole
following interventions for tracking dynamic changes lung, superficial and deep, and allow simple emer-
in pulmonary congestion and decongestion (6). With gency TTE, as well as venous, abdominal, and whole
comprehensive, limited, or focused examinations, body urgent approaches (9).
lung ultrasound is now ready to be embedded in the
TECHNOLOGY. No Doppler, second harmonic, or
standard TTE, from full functionality platforms per-
contrast medium is needed (7), and lung ultrasound is
formed by certified echocardiographers up to pocket
performed at best using simple equipment.
devices used by nonechocardiographers. It is difficult
to find so much diagnostic gain with so little invest- TECHNIQUE. The acoustic window for lung ultra-

ment in terms of technology, training, and time in sound is always patent, even when TTE is not
other areas of cardiology (7). This review is primarily feasible. On the left side of the chest, the lung ultra-
aimed at those caring for cardiology patients (cardi- sound window is close to TTE apical and parasternal
ologists, emergency room physicians, cardiac windows and corresponds to the popular BLUE points
ultrasonographers). in intensivists’ approach (10), where BLUE stands for
bedside lung ultrasonography in emergency (11).
CURRENT METHODOLOGY There are 3 symmetrical regions per lung: 2 anterior
points (upper BLUE point, lower BLUE point); and 1
For the cardiologist, a lung ultrasound study is an posterolateral point, at or behind the posterior axil-
add-on to a TTE study, and it must be focused, fast, lary line, at the level of the lower BLUE point, called
and factual without becoming an extra examination the PLAPS point, where PLAPS stands for posterolat-
requiring excessive additional time, separate eral alveolar and/or pleural syndrome (Figure 1). The
reporting, and supplementary billing. The average anterior BLUE points are sought for the diagnosis of
time of a comprehensive TTE cardiac scan is 40 to 45 pneumothorax and pulmonary edema and are the
min, and we can easily add 1 min more to scan the elective site for detection of pulmonary congestion at
lung for pleural effusion or pulmonary edema. The rest. With stress, there is an additional but important
methodology of a heart-driven lung ultrasound ex- focus on the third intercostal space in the 2 regions
amination can be summarized as follows, regarding between the posterior axillary and anterior axillary
the basic requirements: training, transducer, tech- lines and the anterior axillary and the midclavicular
nology, technique, and targets of examination lines (12), the “wet spots” where lung water accu-
(Table 1). mulates most during semisupine exercise (Figure 2).
TRAINING. The American College of Chest Physicians The PLAPS point allows for immediately diagnosis of
has defined the knowledge and technical elements most pleural effusions (13) and posterior alveolar
required for competence in lung ultrasound (8). In syndromes (14) with >90% sensitivity. The PLAPS
our own experience, 1 morning hands-on experience point is accessible in all patients, including venti-
or even a standardized Internet-based module of 2 h lated, supine, bariatric patients, by using a probe that
is sufficient to achieve excellent reproducibility in can be inserted between this posterolateral part of the
identification and quantification of B-lines, even chest and the bed; the most posterior is the best, but
among lung ultrasound–naive sonographers. They are sometimes this is not easy to access, so the most
among the easiest and most reproducible signs to possible lateral part makes the best compromise for
recognize in cardiovascular ultrasound, considered to detecting PLAPS. Once a pleural effusion is detected,
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Heart-Driven Lung Ultrasound NOVEMBER 2018:1692–705

MAIN SIGNS OF LUNG ULTRASOUND IN


T A B L E 1 Requirements and Technique for Combined TTE and Lung Ultrasound Scanning
PHYSIOLOGY AND DISEASE
Training, Techniques,
and Targets TTE Lung Ultrasound
With lung ultrasound, the lung surface has always a
Training
simple pattern wherever the probe is applied. The
Certification Standardized Deregulated in cardiology
Complexity “University” (complex) “Kindergarten” (easy) whole structure is dynamic and produces physiolog-
Rater variability Good to fair (>20%) Good to excellent (<10%) ical variations in movement from end-inspiration to
Transducer type Cardiac (3.5–5.0 MHz) Cardiac or microconvex 5 MHz end-expiration through the respiratory cycle mirrored
Technology required High-end desirable Simple technology optimal in the pleural movement. The main signs of cardio-
Technique logical interest involve the pleural line, the pleural
Acoustic window 1 Apical PLAPS effusion or consolidation
space, lung motion, the lung interstitium, and the
Acoustic window 2 Parasternal 3 IS, MC, AA, MA for water
lung alveolar space.
Acoustic window 3 Subxiphoid Upper BLUE points for PNT
Patient position Supine Supine or sitting PLEURAL LINE. Normal pattern. The 2 separate
Imaging time 30 min <2 min anatomic structures of parietal and visceral pleura are
Analysis time 10 min <2 min
apposed and, with low-frequency transducers, merge
Emergency setting May reduce data quality Unchanged data quality
into a single pleural line, a 0.2- to 0.3-mm thick
Targets
echogenic, horizontal, smooth specular echo
Target 1, effusion Pericardial effusion Pleural effusion
Target 2, hemodynamics Pulmonary pressures Pulmonary congestion (Figure 3). The reverberation or repetition artifacts
Target 3, others LV and RV systolic function, Interstitial syndrome, behind the pleural line can be horizontal (A-lines) or
diastole, valves, and so on consolidation, PNT vertical (B-lines) images with regular, straight, and
geometric shapes more precisely converging to the
AA ¼ anterior axillary; BLUE ¼ bedside lung ultrasonography in emergency; IS ¼ intercostal space; LV ¼ left
ventricular; MA ¼ midaxillary; MC ¼ midclavicular; PA ¼ posterior axillary; PLAPS ¼ posterolateral alveolar and/ head of the probe (the top of the screen) like parallels
or pleural syndrome; PNT ¼ pneumothorax; RV ¼ right ventricular; TTE ¼ transthoracic echocardiography.
(A-lines) or meridians (B-lines).
Abnormal pattern. In acute respiratory distress syn-
the positive diagnosis is made, and the operator is drome (ARDS) and pneumonia, the fluid exudated by
free to assess the volume of the effusion by moving inflammation is a glue (15), which sticks the lung to
the probe; if no effusion is found, however, time is the parietal pleura, thereby abolishing lung sliding.
spared. Using this simplified approach, lung scanning The pleural line appears thickened and irregular,
can be achieved in far <2 min. For serial examina- possibly because of a small subpleural alveolar syn-
tions, the position (sitting or supine) must be drome (Figure 3). Usually, these static signs come
consistent because pleural and pulmonary lung water together with a single critical dynamic sign, the
changes with posture. Lung ultrasound remains abolition (or severe impairment) of lung sliding. This
feasible and reliable under all hemodynamic and sign is helpful in the differential diagnosis of B-lines
ventilatory conditions, unlike TTE information, in ARDS or pneumonia versus cardiogenic APE (15).
which can deteriorate in acute conditions because of The thickening of the pleural line is the main and
hyperventilation and tachycardia, which make imag- most sensitive sign of lung fibrosis, found, for
ing and interpretation of some parameters (e.g., instance, in rheumatologic disease, and it is best
regional wall motion, diastolic filling) more detected with a high-frequency probe.
challenging. PLEURAL MOVEMENT. Normal pattern. The visceral
TARGETS. For the cardiologist, the main diseases pleura slides over the motionless parietal pleura
targeted by lung ultrasound are characterized by a during breathing. The “lung sliding” is a horizontal,
change in water in the pleural space (pleural effusion) to-and-fro movement, beginning at the pleural line,
or lung parenchyma (pulmonary congestion, at rest synchronous with respiration. There is an obvious
and during stress). In both conditions, lung ultra- vertical gradient in the amplitude of lung sliding,
sound has obvious advantages of sensitivity and which is near zero at the apex and gradually increases
specificity compared with chest radiographs. The up to a maximum near the diaphragm (15). In healthy
BLUE protocol has proposed a standardized approach subjects quietly breathing, the amplitude of lung
to the most common causes of acute respiratory fail- sliding is roughly 10 to 15 mm on the anterior chest
ure, which are in the scope of the cardiologist window at the bases (lower BLUE points).
assessing undifferentiated dyspnea (by decreasing Abnormal pattern. When air separates the 2 pleural
frequency): pneumonia, APE, chronic obstructive layers (pneumothorax), the movement disappears.
pulmonary disease, asthma, pulmonary embolism, When a sticky exudate glues the parietal and the
and pneumothorax (11). visceral pleura (pneumonia, ARDS), the movement is
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F I G U R E 1 The BLUE Points

Posterior
axillary
line

Upper
BLUE-point

Heart
(usual PLAPS
point

ca u a m
location)

lo us rag
tio l
h

n)
ap
Lower

Di
(
BLUE-point
Phrenic line
(usual location)

The bedside lung ultrasonography in emergency (BLUE) points used in the BLUE protocol with the patient in the supine or semirecumbent
position: (left) upper BLUE points and lower BLUE points; (right) posterolateral alveolar and/or pleural syndrome (PLAPS) point. Two hands
(of the size of the patient’s hands, thus allowing universal use in all kinds of patients) applied this way usually cover the anterior lung surface
(note the upper finger applied just below the clavicle). The upper BLUE point is defined using the middle of the upper hand. The lower BLUE
point is defined using the middle of the lower palm. This makes a symmetrical, trapezoid definition that follows the lung anatomy, is usually
far from the heart and the abdominal structures, and keeps clinical value. The lateral continuation of the lower BLUE point, as posterior as
possible behind the posterior axillary line, defines the PLAPS point, always located quite a bit above the diaphragm. Modified with permission
from Lichtenstein and Mezière (10).

reduced or abolished. When collagen bundles bridge and visceral pleura is only a potential space under
the parietal and visceral pleura, the movement is also normal conditions because the 2 pleurae adhere to
reduced, as in pleural adhesions. each other through the few milliliters of serous fluid,
PLEURAL CAVITY. Normal pattern. The fluid-filled thus allowing smooth movement of the visceral
space between the 2 specular reflectors of parietal pleura during the respiratory cycle (Figure 3).

F I G U R E 2 The 4-Sites Simplified Scan for B-Lines

Lung Ultrasound and TTE Windows (Supine Patient)


right side left side
PA MA AA MC PS MS MS PS MC AA MA PA
PA = Posterior-axillary
IS Yellow:
lung water
MA = Mid-axillary at rest and
II˚ after semi-
supine
AA = Anterior-axillary exercise
III˚
MC = Mid-clavicular
IV˚
PS = Para-sternal
V˚ V4 V5 Black:
Parasternal
MS = Margino-sternal
TTE windows
IS = Inter-costal space

The specific spaces (“wet zones”) to look for interstitial lung water accumulation at rest and after stress with the 4-sites simplified scan. TTE ¼
transthoracic echocardiography. Modified with permission from Scali et al. (12).
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F I G U R E 3 Lung Ultrasound Normal and Abnormal Patterns

Regular pleural line,


A-lines
B-lines

Large pleural
Irregular pleural line,
effusion, lung
B-lines
consolidation

(Upper left) Normal lung surface. The pleural line is thin, and the interstitial tissue does not generate any signal, so all that is seen using
ultrasound is the repetition of the pleural line (A-lines). The A-line indicates air below the pleural line (alveolar, or pneumothorax). If this
pattern is associated, anteriorly and symmetrically, with lung sliding, the air is alveolar gas, and this pattern is called the A profile. At the
posterolateral alveolar and/or pleural syndrome (PLAPS) point, no PLAPS is seen in the normal lung surface, usually A-lines (with lung
sliding), sometimes B-lines are seen. (Upper right) The pulmonary congestion pattern, with a perfectly visible normal pleural line and 4
B-lines. Together with lung sliding (which cannot be appreciated from the frozen frame), if it is anterior, bilateral, symmetrical, this pattern
defines the B profile. (Lower left) Large pleural effusion, with a fully consolidated lower lobe at the posterolateral alveolar and/or pleural
syndrome point. (Lower right) At the anterior bedside lung ultrasonography in emergency (BLUE) points, the pleural line is irregular and
thickened, usually indicating pneumonia and/or acute respiratory distress syndrome.

Abnormal pattern. The pleural effusion noted by ul- one another below the pleura, at exact multiples of
trasound is characterized by the static sign of a space the transducer-pleural line (Figure 3). A-lines indicate
between the pleural line and the lung line (always that there is air below the pleural line, either 99.5%
regular, roughly parallel to pleural line, which shows air (i.e., normal lung below, which contains trace
the visceral pleura) (Figure 3). The dynamic sign is a amount of water) or 100% air (in pneumothorax) (14).
variation of this interpleural space within the respi- Abnormal interstitial pattern: multiple B-lines. The B line
ratory cycle, with the inspiratory displacement of the is defined according to 7 criteria: 3 constant and 4
lung line toward the pleural line and maximal dis- almost constant. The B-line is constantly a comet-tail,
tance at end-expiration. The static sign is called the vertical artifact. Constantly, it arises from the pleural
“quad sign,” and the dynamic sign is the “sinusoid line. Constantly, it moves in sync with lung sliding
sign” (15). Transudative effusions are anechoic (echo (when there is lung sliding). Quasi-constantly, the B-
free). Exudates can be anechoic or echoic, the most line is well defined and laser-like; long, extending to
severe cases being usually perfectly echoic (empy- the bottom of the screen without fading; erasing A-
ema, hemothorax). lines; and hyperechoic. This precise definition allows
LUNG PARENCHYMA. Normal pattern. The normal universal recognition in all cases (Figure 3). B-line is
lung shows lung sliding with A-lines, which are arti- now the preferred name, but these lines are also
factual horizontal reverberations, equidistant from called ultrasound lung comets. More than 2 B-lines
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per intercostal space have been called lung rockets pleural effusion only after pulmonary edema has
(15). In some locations, 1 or 2 B-lines are physiolog- developed (16,17). Elevated right atrial pressure in
ical, for instance, anteriorly corresponding to lung right-sided heart failure can increase the pressure in
fissures or lung rockets at the bases (likely natural the thoracic duct, thus limiting the volume of
gravity). Ultrasound interstitial syndrome is defined lymphatic drainage from the pleural space to the right
by lung rockets. It can be diffuse at the whole chest atrium through the superior vena cava (16–19).
wall or symmetrical and associated with conserved BEDSIDE RECOGNITION. The main signs on physical
lung sliding in the case of cardiogenic APE. This very examination are reduced air entry and dullness to
precise pattern is called the B profile in the BLUE percussion at lung bases (20). In up to 20% of pa-
protocol (11). It can be diffuse but associated with tients with acute heart failure (AHF), the chest
abolished or very decreased lung sliding and labeled radiograph is nearly normal, and the sensitivity of
the B0 profile (11) in some cases of pneumonia and/or the method is less than one-half compared with lung
ARDS. It can be localized, usually in infectious or in- ultrasound, especially for mild to moderate pleural
flammatory processes (pneumonia, ARDS), and effusions (20).
labeled the A/B profile.
Ultrasound multiple B-lines are the equivalent of METHODOLOGY. Semiquantitative grading of the
the radiological interstitial syndrome (Kerley lines amount of pleural effusion is possible by measuring
and more). We see interstitial syndrome, in acute the maximal expiratory interpleural distance from the
conditions, in 2 main diagnoses with opposed man- pleural line to the lung line on the posterior axillary
agement: cardiogenic APE and pneumonia or ARDS. line with the patient in the supine position (13) or the
Cardiogenic APE is associated with normal lung paravertebral, scapular, posterior axillary, or medial
sliding, which is often reduced or abolished in axillary lines in the sitting position (21). The amount
pneumonia or ARDS. of pleural effusion can be scored as trivial (<2 mm),
B-lines must not be mixed up with Z-lines, which small (2 to 15 mm, too small to tap), moderate (15 to 25
are frequently observed as bundle-shaped reflections mm), or large (>25 mm) (Table 2).
arising from the pleural line, but that—unlike true B- DIAGNOSTIC, PROGNOSTIC, AND THERAPEUTIC
lines—do not erase A-lines, are ill-defined, are less IMPLICATIONS. The prevalence of pleural effusion
echogenic than the pleural line, are short, and do not may range anywhere between 56% and 90% in AHF,
move in synchrony with respiration (15). 30% and 60% at pre-discharge, 10% and 70% in
Abnormal alveolar pattern: lung consolidation. In some outpatients with chronic stable heart failure, or
conditions, the extreme progression of the interstitial 25% in patients with isolated right-sided heart failure
syndrome leads to the consolidation process with an (10,21–31) (Table 3). The main TTE predictor of
echogenic lung, with a tissue texture similar to that of pleural effusion is the increased systolic pulmonary
spleen or liver, the result of replacement of air in the arterial pressure (31).
alveolar space with material other than air, usually In patients with heart failure, the presence of
water, pus, or blood (15) (Figure 3). Lung consolida- pleural effusion is associated with a higher rehospi-
tion can have a variety of causes, including alveolar talization rate (26) and clearly worse quality of life,
cardiogenic APE, pneumonia, lung infarction, cancer, which has improved after reduction of pleural
lung contusion, and obstructive atelectasis. In some effusion with medical therapy (30). In patients with
etiologies, such as drowning or aspiration pneumo- AHF and pleural effusion, thoracentesis with fluid
nitis, the fluid comes directly to fill the alveoli first, evacuation may be considered if feasible to alleviate
and the initial presentation is lung consolidation, dyspnea (20). For thoracentesis, a $15-mm inter-
without the usual initial phase of interstitial syn- pleural inspiratory distance is required (13); the nee-
drome. Lung consolidations may arise in any site, dle is inserted after careful check that 6 organs are not
and, although only the peripheral part of the lungs in the pathway of the needle: the diaphragm, of
can be visualized by ultrasound, 98.5% of consolida- course, but also the heart, descending aorta, spleen,
tions touch the pleura, and 90% of cases locate at the liver, and lung. The quantification is especially
PLAPS point (14). important for assessing variations in the same patient
in natural history or following intervention. Lung
PLEURAL EFFUSION IN HEART FAILURE ultrasound is ideal for guiding thoracentesis and
draining effusions. The absence of a virtual space
PATHOPHYSIOLOGICAL MEANING. Elevated left after the procedure (interpleural space >10 mm) re-
atrial pressure in left-sided heart failure may cause flects an incomplete procedure.
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knows that the patient can have cardiogenic APE,


T A B L E 2 Pericardial and Pleural Effusions: Similarities and Differences by Ultrasound
ARDS or pneumonia, or, rarely, any chronic intersti-
Pericardial Pleural tial disease. The physician will use the profiles of the
Measurements Effusion Effusion
BLUE protocol for refining the diagnosis: lung sliding
TTE, descending aorta Anterior Posterior
associated, making at the anterior wall the B profile,
Temporal change With cardiac cycle With respiratory cycle
Spatial change (supine-sitting) Absent Present
highly accurate for cardiogenic APE; or lung sliding
Where to measure Parasternal apical views PLAPS point abolished, making the B 0 profile, highly specific to
Pathophysiology in HF Right atrial hypertension Right or left atrial hypertension pneumonia or ARDS. In spite of these caveats, the
Normal value of serosal fluid <50 ml <25 ml (for each lung) technique is now the best available for bedside
Size detection of pulmonary congestion.
Trivial Only systolic <2 mm
METHODOLOGY. The comprehensive 28-site scan on
Small <10 mm (50–100 ml) 2–15 mm (too small to tap)
Moderate 10–20 mm (100–500 ml) 15–25 mm the anterolateral chest was initially proposed in a
Large >20 mm (>500 ml) >25 mm (>500 ml) cardiologic setting in 2004 (3) and adopted in
research studies, but it was still too time-consuming
HF ¼ heart failure; other abbreviations as in Table 1.
for routine use in real-world laboratories, especially
during stress echocardiography, when the time pres-
sure is higher (7). Similar information can be obtained
PULMONARY CONGESTION
in much less time with a simplified 4-site scan,
including only the “wet spots” with most B-lines
PATHOPHYSIOLOGICAL MEANING. The sequence of
(Figure 2). In this way lung ultrasound mapping does
events leading to APE during heart failure can be
not interfere with electrocardiographic leads and
conceptualized as a cascade—the so-called lung water
takes only 20 s to be completed (10–12).
cascade—whose sequence was unveiled with the
advent of lung ultrasound (32). The initiating events DIAGNOSTIC, PROGNOSTIC, AND THERAPEUTIC
of the cascade are the increases in left ventricular IMPLICATIONS. AHF accounts for about 1 million
end-diastolic pressure and pulmonary capillary emergency department visits in the United States,
wedge pressure (hemodynamic congestion), eventu- and even when cardiac peptides are incorporated into
ally leading to the imbalance of Starling’s equilibrium the clinical work-up of acute dyspnea, the misclassi-
in the alveolar capillary barrier, which is the pre- fication rate remains at 14% to 29% (37). As shown by
requisite for increased accumulation of lung water a recent meta-analysis recruiting 1,914 patients (37),
(Figure 4). In between hemodynamic and clinical the B profile identifies the cardiogenic origin of dys-
pulmonary congestion, the intermediate event is pnea with 85% sensitivity and 92% specificity (11,37–
interstitial pulmonary congestion detectable by lung 49), superior to pleural effusion and TTE (Table 4),
ultrasound as multiple B-lines (33), linked bio- and comparable to cardiac natriuretic peptides (37–
physically to an increased water-to-air ratio per unit 41). The variability of reported specificities (ranging
of lung volume tissue in the subpleural interlobular from 45% to 97%) likely reflects the selection criteria
septa (7). adopted in the different studies, with high pre-test
BEDSIDE RECOGNITION. Pulmonary congestion is probability of cardiogenic origin in critically ill pa-
the key manifestation of impending AHF, but the tients admitted to intensive care units (11) and low to
clinical, auscultatory, and chest radiographic findings intermediate pre-test probability in clinically stable
are all late, insensitive, and unspecific signs of pul- patients evaluated on admission to the emergency
monary congestion (34). The reproducibility of the department (38).
findings is poor for crackles and moderate for chest The B profile is useful to track dynamic changes in
radiography, but high for B-lines (35). Quantification pulmonary congestion in response to treatment
is easier and more effective for lung ultrasound, and (3,36), and its persistence at pre-discharge or in clin-
it is based on the number of B-lines per space and ically stable outpatients with heart failure is predic-
spatial extension. Changes in B-lines are very quick to tive of heart failure hospitalization or death (22–30).
appear (for instance, during exercise or a volume The key question is whether B profile can be used
challenge) and to disappear (for instance, with di- as a surrogate endpoint to guide interventions, such
uretics or dialysis), and therefore they must be as increase in diuretic therapy in patients with heart
interpreted in view of previous interventions (36). failure or of dialysis rate in patients with advanced
Multiple B-lines (lung rockets) are not designed for chronic kidney disease. Several large-scale random-
identifying a disease, but rather a syndrome: inter- ized studies are in progress (NCT02310061,
stitial syndrome. From this basis, the physician NCT03262571, NCT02959372, NCT03136198).
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NOVEMBER 2018:1692–705 Heart-Driven Lung Ultrasound

T A B L E 3 Lung Ultrasound in Left- and Right-Sided Heart Failure

First Author, Pleural


Year (Ref. #) Patients Effusion B Profile Main Finding

Morales-Rull, 2018 (31) 3,245 AHF inpatients 56% N/A SPAP >55 mm Hg predicts pleural effusion
Gundersen, 2017 (30) 62 CHF outpatients 42% N/A Pleural effusion predicts quality of life
Scali, 2017 (10) 103 CHF patients N/A 58% B profile predicts events
Miglioranza, 2017 (29) 97 CHF outpatients N/A 68% B profile predicts events
Platz, 2016 (28) 185 CHF outpatients N/A 32% B profile predicts events
Cogliati, 2016 (27) 149 AHF pre-discharge 36% 64% B profile predicts events
Gustaffson, 2015 (26) 104 CHF outpatients 10% 27% Pleural effusion and B profile predict events
Coiro, 2015 (25) 60 AHF pre-discharge N/A 30% B profile predicts readmission
Gargani, 2015 (24) 99 AHF pre-discharge 24% 40% B profile predicts readmission
Zoccali, 2013 (23) 392 patients undergoing hemodialysis N/A 59% B profile predicts death
Luo, 2011 (19) 89 patients with connective tissue disease 39%* N/A Pleural effusion with RHF
Tang, 2009 (18) 147 patients with PAH 21%* N/A Pleural effusion with RHF
Lichtenstein, 2008 (11) 64 patients with acute respiratory failure N/A 97% Patients in ICU
Frassi, 2007 (22) 290 inpatients (chest pain or dyspnea) N/A 47% B profile predicts events
Jambrik, 2004 (3) 121 CCU inpatients 15%† 68% SPAP and E/e0 predict B profile
Kataoka, 2000 (21) 60 AHF inpatients 91% N/A 41% with pleural effusion by chest radiograph
Wiener-Kronish, 1985 (17) 37 AHF inpatients 51% N/A Left atrial pressure higher in pleural effusion

*Chest radiograph, computed tomography, lung ultrasound, or autopsy. †Chest radiograph.


AHF ¼ acute heart failure; CCU ¼ coronary care unit; CHF ¼ chronic heart failure; ICU ¼ intensive care unit; N/A ¼ not available; PAH ¼ pulmonary arterial hypertension;
RHF ¼ right-sided heart failure; SPAP ¼ systolic pulmonary arterial pressure.

Lung ultrasound is a useful adjunct to TTE dur- different sign (B-lines rather than regional wall
ing stress echocardiography (10,50,51), by providing motion abnormalities), and in a different time
information on a different pathophysiological target window (after rather than at peak stress). As a
(alveolar-capillary barrier rather than physiologi- parameter, B-lines are more feasible, simpler to
cally critical epicardial artery stenosis), with a image and to measure, and inherently more

F I G U R E 4 The Lung Water Cascade

THE LUNG WATER CASCADE


Stable Chronic Heart Failure
Events

Wedge pressure rise Starling equation unbalance Asymptomatic hemodynamic congestion

STRESS Stress B-lines


Lung Ultrasound
Asymptomatic pulmonary congestion

REST B-lines
Lung Ultrasound

SYMPTOMS/SIGNS Clinical congestion


Crackles/Dyspnea/Weight gain

Acute decompensated Heart Failure

Time
(hours, days or weeks)

Hemodynamic congestion is the early event before the imaging sign (multiple B-lines) of pulmonary congestion. Stress B-lines are an earlier
event than resting B-lines. Only after hours, days, or weeks is the clinical congestion apparent. The therapeutic countermeasures are likely
more effective when initiated at the early, pre-symptomatic and pre-radiologic, silent stages of the cascade.
1700 Picano et al. JACC: CARDIOVASCULAR IMAGING, VOL. 11, NO. 11, 2018

Heart-Driven Lung Ultrasound NOVEMBER 2018:1692–705

quantitative than regional wall motion. The accu-


T A B L E 4 Lung Ultrasound to Identify Acute Heart Failure in
Patients With Dyspnea
mulation of lung water during exercise is correlated
with more advanced functional forms of heart
First Author, B Profile
Year (Ref. #) N (S, Sp) TTE
failure and worse prognosis in patients with heart
Ohman, 2017 (49) 100 100, 95 0
E/e >15
failure with reduced ejection function (10), and it is
Sforza, 2017 (48) 68 92, 80 EF <40%, IVC found also in patients with heart failure and
Pivetta, 2015 (47) 1,005 97, 97 N/A preserved ejection fraction (51) (Figure 5, Online
Russell, 2015 (46) 99 69, 83 EF <45% Video 1).
Anderson, 2013 (45) 101 70, 75 EF <40%, IVC
Cibinel, 2012 (44) 56 94, 84 N/A
PULMONARY EMBOLISM
Vitturi, 2011 (43) 152 97, 75 Larger EDV, lower EF
Prosen, 2011 (42) 248 100, 95 N/A
Lung ultrasound usually shows normal anterior
Nazerian, 2010 (41) 145 N/A Dt, EF <50%
Wang, 2010 (40) 84 N/A EDV, EF A-lines and lung sliding (i.e., A profile), often
Liteplo, 2009 (39) 100 58, 85 N/A accompanied by posterior lung consolidation and
Gargani, 2008 (38) 149 97, 45 N/A pleural effusion (11). Venous ultrasonography (with
Lichtenstein, 2008 (11) 301 97, 95 N/A compression in cases when thrombosis is not seen
directly) shows deep vein thrombosis with good
Dt ¼ deceleration time of E wave <130 ms on pulsed Doppler analysis of mitral
inflow; EDV ¼ end-diastolic volume; IVC ¼ inferior vena cava with diameter >2.0 sensitivity (11). TTE may detect (with high speci-
cm and variation of size with breathing <50%; S ¼ sensitivity; Sp ¼ specificity;
ficity but low sensitivity) prognostically relevant
other abbreviations as in Tables 1 and 3.
right ventricular overload and, rarely, the

F I G U R E 5 Stress Lung Ultrasound Patterns

TTE-Lung Ultrasound Stress Echo

NON-ISCHEMIC HEART ISCHEMIC HEART

RWMA

DRY LUNG WET LUNG

B-lines

CAD HFrEF HFpEF Aortic Valve Disease Mitral Valve Disease Extreme Physiology HCM

The results of dual imaging (transthoracic echocardiography [TTE] and lung ultrasound) during stress echocardiography (stress echo) identify
any combination of transthoracic echocardiography and lung ultrasound findings: ischemic (with regional wall motion abnormalities) or non-
ischemic heart by transthoracic echocardiography; and dry (with A-lines) or wet (with acute increase of B-lines) lung by lung ultrasound (with
cardiac probe). In the box in the middle, the estimated relative frequency of different patients observed in a high-volume stress echocardi-
ography laboratory with potential sources of stress B-lines. Also see Online Video 1. CAD ¼ coronary artery disease; HCM ¼ hypertrophic
cardiomyopathy; HFpEF ¼ heart failure with preserved ejection fraction; HFrEF ¼ heart failure with reduced ejection fraction; RWMA ¼ regional
wall motion abnormality.
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NOVEMBER 2018:1692–705 Heart-Driven Lung Ultrasound

T A B L E 5 Wet Versus Dry B-Lines T A B L E 6 Differential Diagnosis of Cardiogenic APE Versus ARDS

Feature Wet (Water) Dry (Fibrosis) Feature Cardiogenic APE ARDS

Pleural line Regular, thin Irregular, thickened Multiple B-line distribution Anterior diffuse* Sometimes random†
Pleural movement Normal sliding Reduced sliding Right and left lung Symmetrical Sometimes spared areas†
Pleural effusion Frequent, bilateral Only trivial Anterior pleural line Regular, thin Sometimes irregular, thickened‡
From supine to upright Decrease (s) No change Pleural movement Normal sliding Sometimes reduced sliding§
Exercise Increase (min) No change Pleural effusion Frequent, bilateral Sometimes present
Diuretics Decrease (h) No change Dependent consolidation Usually present Usually present
Nondependent (anterior) Never visible Sometimes present
consolidation
TTE, LV function Severely abnormal Often normal
pathognomonic sign of a mobile serpentine
thrombus in the right side of the heart or the pul- *Corresponds to the B profile of the BLUE protocol. †Corresponds to the A/B profile of the BLUE protocol.
monary artery. Triple ultrasound imaging of heart, ‡Corresponds to the C profile of the BLUE protocol. §Corresponds to the B0 profile of the BLUE protocol.
APE ¼ acute pulmonary edema; ARDS ¼ acute respiratory distress syndrome; other abbreviations as in Table 1.
lung, and veins may have a role as a first-line add-
on to clinical probability scores and D-dimer testing
(52). translate into specific diagnosis of disease (Table 7),
PRIMARY PULMONARY DISEASES: obviously after integration with the clinical presen-
INTERSTITIAL LUNG DISEASES, tation, TTE, venous ultrasonography for deep vein
PNEUMONIA AND ARDS, PNEUMOTHORAX thrombosis detection, and others.

LUNG ULTRASOUND IN SCIENTIFIC


Different primary pulmonary diseases are present as SOCIETIES’ RECOMMENDATIONS
comorbidities in heart failure or as causes of dyspnea
suspected to be cardiac in origin. Lung ultrasound is Ultrasound guidance has been “strongly recom-
helpful in recognizing these diseases. mended” since 2010 by the British Thoracic Society
Pulmonary interstitial fibrosis with lung rockets for all pleural procedures with pleural fluid because it
accompanied by a thickened or irregular pleural line is associated with a lower failure rate and rate of
can be found in 20% to 50% of patients with systemic complications such as pneumothorax and bleeding
sclerosis and, less frequently, in other rheumatologic (56). It is becoming increasingly difficult to justify
diseases (53). Fibrotic (“dry”) B-lines are not performing these procedures without ultrasound
increased by exercise or decreased by upright posi- guidance (57).
tion or diuretic challenge (Table 5). European Association of Cardiovascular Imaging
With lung ultrasound, pneumonia and ARDS recommendations for use of pocket-size devices
appear, roughly, as a single entity (11,54). ARDS can explicitly list “semi-quantification of extra-vascular
be separated from cardiogenic APE on the basis of lung water” with B profile among the top 8 in-
several lung ultrasound and TTE features, summa- dications (58). In emergency echography, the absence
rized in Table 6. of B profile excludes cardiogenic edema with a
As opposed to what happens for water in pleural
effusion, in pneumothorax air tends to accumulate
according to antigravity laws in the least dependent T A B L E 7 From Lung Ultrasound Signs to Specific Diseases
part of the chest. The ultrasound diagnosis of pneu-
Lung Pleural Line Pleural Anterior Lung
mothorax is based on 2 sequential signs. The first is Diagnosis BLUE Profile Sliding Changes Effusion Consolidation Point
the anterior detection of abolished lung sliding with AHPE B þ  þ  
the complete absence of B-line (called A 0 profile in the Pneumonia or ARDS B’, A/B, C, PLAPS  þ þ  
BLUE protocol). The second sequential sign, to be Pulmonary embolism A with DVT þ  þ  
sought only in presence of an A 0 profile, is the Pneumothorax A’     þ
COPD or asthma Nude þ    
detection of the lung point, defined as the sudden
0 ILF B, B’, C  þ   
replacement of the A profile by any other pattern,
usually lung sliding or B-lines (11,55). Terminology modified from the BLUE protocol (11): A profile ¼ normal anterior A-lines and lung sliding; A’
profile ¼ anterior A-lines and abolished lung sliding (plus lung point ¼ pneumothorax); B profile ¼ diffuse
FROM LUNG ULTRASOUND SIGNS TO anterior B-lines and preserved lung sliding; B’ profile ¼ diffuse anterior B-lines and reduced lung sliding; A/B
profile ¼ mixed and balanced A and B profiles; C profile ¼ anterior lung consolidation; nude profile ¼ everything
SPECIFIC DISEASES normal.
AHPE ¼ acute hemodynamic pulmonary edema; COPD ¼ chronic obstructive pulmonary disease; DVT ¼ deep
vein thrombosis at venous ultrasonography; ILF ¼ interstitial lung fibrosis; þ ¼ present,  ¼ absent or reduced;
Different diseases can be identified by lung ultra- other abbreviations as in Table 1.
sound on the basis of the main signs that may
1702 Picano et al. JACC: CARDIOVASCULAR IMAGING, VOL. 11, NO. 11, 2018

Heart-Driven Lung Ultrasound NOVEMBER 2018:1692–705

C E NT R AL IL L U STR AT IO N The Shape of Lung Water

Picano, E. et al. J Am Coll Cardiol Img. 2018;11(11):1692–705.

(Center) The normal pattern seen by transthoracic echocardiography and lung ultrasound, with (top center) normal left-sided filling pressures (normal mitral inflow
pattern with E/A ratio >1), (middle center) normal right-sided filling pressures (inferior vena cava diameter <21 mm, collapsing >50% with a sniff); and (bottom
center) A profile (with A-lines at the anterior chest wall) at lung ultrasound. (Right) The left-sided heart failure pattern seen by transthoracic echocardiography and
lung ultrasound, with (top right) increased left-sided filling pressures (E-wave deceleration time <160 ms with restrictive filling pattern), (middle right) B profile, and
(bottom right) pleural effusion. (Left) The right-sided heart failure pattern seen by transthoracic echocardiography and lung ultrasound. Transthoracic echocar-
diography shows increased right-sided pressures: (top left) tricuspid regurgitant jet at color Doppler; (middle left) systolic pulmonary arterial pressure is 67 mm Hg,
estimated with continuous-wave Doppler from tricuspid regurgitant jet velocity. (Bottom left) Lung ultrasound shows pleural effusion. White asterisks indicate the
pleural line. On the aligned M-mode image, the upper stratified pattern is separated by the lower sandy pattern by the pleural line.

negative predictive value close to 100% (11,59). The diagnostic test to assess pulmonary congestion in
2016 guidelines on heart failure of the European suspected AHF because “in reasonably expert hands
Society of Cardiology recommend lung ultrasound it can be equally or more informative than chest X-ray
among diagnostic tests in heart failure (Class IIb, allowing also an important time-saving” (60). The
Level of Evidence: C) as a test that may be considered 2017 expert consensus of the AHF group of the Eu-
in patients with AHF to confirm pulmonary conges- ropean Society of Cardiology concluded that “TTE
tion and pleural transudate (20). In patients with and lung ultrasound can assist in the rapid assess-
AHF, in 2015 lung ultrasound was recommended by ment of patients with acute dyspnea and hypotension
the European Society of Cardiology as a first-line and have the potential to transform the way in which
JACC: CARDIOVASCULAR IMAGING, VOL. 11, NO. 11, 2018 Picano et al. 1703
NOVEMBER 2018:1692–705 Heart-Driven Lung Ultrasound

the clinicians assess and manage critically ill patients findings using experience, prudence, and clinical
with AHF and cardiogenic shock” (61). wisdom is always necessary.
According to the 2016 joint European Association Large scale, prospective, international, multi-
of Cardiovascular Imaging and American Society of center, effectiveness studies are currently ongoing
Echocardiography recommendations, during exercise with rest and stress B-lines in known or suspected
stress echocardiography the acute increase in B-lines heart failure and coronary artery disease in the Stress
detected by lung ultrasound is a feasible way for Echo 2020 study, which is planning to recruit 10,000
demonstrating that the symptom “dyspnea when patients within the year 2020 with the new standard
exercising” is related to pulmonary congestion sec- of dual imaging, including regional wall motion and
ondary to backward heart failure (62). B-lines (64).
Randomized outcome studies are needed to assess
CURRENT LIMITATIONS the value of lung ultrasound are needed to reduce
mortality in patients with either chronic heart failure
Severe subcutaneous emphysema can be an absolute or acute circulatory failure.
hindrance. Dressings should be limited for favoring
CONCLUSIONS
ultrasound studies. Morbid obesity is not a limitation
for several areas of lung ultrasound, mainly detection
After opening the acoustic window on lung paren-
of A profile, A 0 profile, B profile, and B 0 profile (15).
chyma, the cardiologist discovers unique information
Lung rockets reflect the presence of an interstitial
that will soon induce a durable mutation in the
syndrome that can be caused by water, inflamma-
structure of cardiac ultrasound examination,
tion, or fibrosis, but integration with clinical
destined to become a cardiopulmonary (TTE-lung
presentation, systematic application of lung ultra-
ultrasound) study. Now is the appropriate time for
sound with the BLUE protocol, and association with
professional cardiology and echocardiography
TTE allow the clinician to identify the underlying
societies to incorporate lung ultrasound into the
etiologic factors and to answer the clinical question
mainstream of core teaching, certification, and
most of the time (11).
reporting in TTE. Lung ultrasound can provide
Lung ultrasound is currently used by many
unique information in the cardiology ward, intensive
different medical disciplines, from cardiology to
care unit, emergency room, echocardiography labo-
intensive care, from pneumology to nephrology, from
ratory, stress testing laboratory, outpatient clinic,
rheumatology to sports medicine. This range adds
and perhaps especially in home care with handheld
appeal to the technique, but it may pose communi-
devices in patients with heart failure (Central Illus-
cation difficulties related to heterogeneity of
tration). The use of lung ultrasound will reduce the
terminology, execution, and reporting, and better
use of techniques based on ionizing radiation, such as
harmonization is needed (7). For the past 3 decades,
chest radiography or computed tomography, thereby
standardized labels for lung ultrasound have been
contributing to minimize the cumulative burden of
refined for maximal efficiency in a field made free of
unwanted effects of radiation exposure, especially
any confusion (11,15).
relevant in cardiology patients (65). A “wet lung”
Lung ultrasound can reduce medicolegal risk by
detected as B profile by lung ultrasound, at rest or
shortening the time to diagnosis in patients with life-
after stress, in a stable patient with chronic heart
threatening conditions. The best defense against
failure predicts impending AHF decompensation and
litigation is to follow training strictly. Malpractice
may trigger lung decongestion therapy. No cardiolo-
lawsuits have been filed for not performing the ex-
gist would evaluate a patient with heart failure
amination in a timely manner (63).
without listening to lung fields for crackles or a
PERSPECTIVES pleural effusion. In the same way, today no compre-
hensive, limited, or focused TTE examination will be
The image texture is, at least in principle, suitable for considered complete without a short but efficient
treatment with video-densitometric analysis, and assessment of the lung.
lung water software is already included in some
commercially available instruments to provide ADDRESS FOR CORRESPONDENCE: Dr. Eugenio Pic-
quantitative support to B-line reading. This option is ano, Institute of Clinical Physiology, Italian National
attractive, but as in any field, and especially in im- Research Council, Via Moruzzi 1, 56124 Pisa, Italy.
aging, checking the quantitative, machine-generated E-mail: picano@ifc.cnr.it.
1704 Picano et al. JACC: CARDIOVASCULAR IMAGING, VOL. 11, NO. 11, 2018

Heart-Driven Lung Ultrasound NOVEMBER 2018:1692–705

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